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      Invasive Snails and an Emerging Infectious Disease: Results from the First National Survey on Angiostrongylus cantonensis in China

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          Abstract

          Background

          Eosinophilic meningitis (angiostrongyliasis) caused by Angiostrongylus cantonensis is emerging in mainland China. However, the distribution of A. cantonensis and its intermediate host snails, and the role of two invasive snail species in the emergence of angiostrongyliasis, are not well understood.

          Methodology/Principal Findings

          A national survey pertaining to A. cantonensis was carried out using a grid sampling approach (spatial resolution: 40×40 km). One village per grid cell was randomly selected from a 5% random sample of grid cells located in areas where the presence of the intermediate host snail Pomacea canaliculata had been predicted based on a degree-day model. Potential intermediate hosts of A. cantonensis were collected in the field, restaurants, markets and snail farms, and examined for infection. The infection prevalence among intermediate host snails was estimated, and the prevalence of A. cantonensis within P. canaliculata was displayed on a map, and predicted for non-sampled locations. It was confirmed that P. canaliculata and Achatina fulica were the predominant intermediate hosts of A. cantonensis in China, and these snails were found to be well established in 11 and six provinces, respectively. Infected snails of either species were found in seven provinces, closely matching the endemic area of A. cantonensis. Infected snails were also found in markets and restaurants. Two clusters of A. cantonensis–infected P. canaliculata were predicted in Fujian and Guangxi provinces.

          Conclusions/Significance

          The first national survey in China revealed a wide distribution of A. cantonensis and two invasive snail species, indicating that a considerable number of people are at risk of angiostrongyliasis. Health education, rigorous food inspection and surveillance are all needed to prevent recurrent angiostrongyliasis outbreaks.

          Author Summary

          Eosinophilic meningitis is caused by the rat lungworm ( Angiostrongylus cantonensis). This parasite is endemic in Southeast Asia, Australia, the Caribbean, and on Pacific Islands. Moreover, the disease is emerging in mainland China, which might be related to the spread of two invasive snail species ( Achatina fulica and Pomacea canaliculata). Thus far, the biggest angiostrongyliasis outbreak in China occurred in 2006 in Beijing, involving 160 patients. However, detailed information about the national distribution of A. cantonensis and its intermediate hosts is still lacking, and the importance of the two invasive snail species for disease transmission is not well understood. Therefore, a national survey on the distribution of A. cantonensis and its intermediate hosts in China was carried out in 2006/2007. It was found that A. fulica and P. canaliculata were implicated in most angiostrongyliasis outbreaks, and that the distribution of A. cantonensis closely matched that of these snails. The two invasive snail species facilitated the expansion of the parasite, thus probably leading to the emergence of angiostrongyliasis, a previously rare disease, in mainland China.

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          Most cited references 63

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          Factors in the emergence of infectious diseases.

           S. S. Morse (1995)
          "Emerging" infectious diseases can be defined as infections that have newly appeared in a population or have existed but are rapidly increasing in incidence or geographic range. Among recent examples are HIV/AIDS, hantavirus pulmonary syndrome, Lyme disease, and hemolytic uremic syndrome (a foodborne infection caused by certain strains of Escherichia coli). Specific factors precipitating disease emergence can be identified in virtually all cases. These include ecological, environmental, or demographic factors that place people at increased contact with a previously unfamiliar microbe or its natural host or promote dissemination. These factors are increasing in prevalence; this increase, together with the ongoing evolution of viral and microbial variants and selection for drug resistance, suggests that infections will continue to emerge and probably increase and emphasizes the urgent need for effective surveillance and control. Dr. David Satcher's article and this overview inaugurate Perspectives, a regular section in this journal intended to present and develop unifying concepts and strategies for considering emerging infections and their underlying factors. The editors welcome, as contributions to the Perspectives section, overviews, syntheses, and case studies that shed light on how and why infections emerge, and how they may be anticipated and prevented.
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            Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions.

            The spread of exotic species and climate change are among the most serious global environmental threats. Each independently causes considerable ecological damage, yet few data are available to assess whether changing climate might facilitate invasions by favoring introduced over native species. Here, we compare our long-term record of weekly sessile marine invertebrate recruitment with interannual variation in water temperature to assess the likely effect of climate change on the success and spread of introduced species. For the three most abundant introduced species of ascidian (sea squirt), the timing of the initiation of recruitment was strongly negatively correlated with winter water temperature, indicating that invaders arrived earlier in the season in years with warmer winters. Total recruitment of introduced species during the following summer also was positively correlated with winter water temperature. In contrast, the magnitude of native ascidian recruitment was negatively correlated with winter temperature (more recruitment in colder years) and the timing of native recruitment was unaffected. In manipulative laboratory experiments, two introduced compound ascidians grew faster than a native species, but only at temperatures near the maximum observed in summer. These data suggest that the greatest effects of climate change on biotic communities may be due to changing maximum and minimum temperatures rather than annual means. By giving introduced species an earlier start, and increasing the magnitude of their growth and recruitment relative to natives, global warming may facilitate a shift to dominance by nonnative species, accelerating the homogenization of the global biota.
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              Predicting the global spread of H5N1 avian influenza.

              The spread of highly pathogenic H5N1 avian influenza into Asia, Europe, and Africa has resulted in enormous impacts on the poultry industry and presents an important threat to human health. The pathways by which the virus has and will spread between countries have been debated extensively, but have yet to be analyzed comprehensively and quantitatively. We integrated data on phylogenetic relationships of virus isolates, migratory bird movements, and trade in poultry and wild birds to determine the pathway for 52 individual introduction events into countries and predict future spread. We show that 9 of 21 of H5N1 introductions to countries in Asia were most likely through poultry, and 3 of 21 were most likely through migrating birds. In contrast, spread to most (20/23) countries in Europe was most likely through migratory birds. Spread in Africa was likely partly by poultry (2/8 introductions) and partly by migrating birds (3/8). Our analyses predict that H5N1 is more likely to be introduced into the Western Hemisphere through infected poultry and into the mainland United States by subsequent movement of migrating birds from neighboring countries, rather than from eastern Siberia. These results highlight the potential synergism between trade and wild animal movement in the emergence and pandemic spread of pathogens and demonstrate the value of predictive models for disease control.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                February 2009
                10 February 2009
                : 3
                : 2
                Affiliations
                [1 ]National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China
                [2 ]Department of Public Health and Epidemiology, Swiss Tropical Institute, Basel, Switzerland
                [3 ]Ministry of Health of China, Beijing, People's Republic of China
                Biomedical Research Institute, United States of America
                Author notes

                Conceived and designed the experiments: SL YZ ZC LYW XNZ. Performed the experiments: SL YZ HXL LH KY. Analyzed the data: SL KY. Contributed reagents/materials/analysis tools: SL YZ. Wrote the paper: SL PS JU XNZ.

                Article
                08-PNTD-RA-0335R2
                10.1371/journal.pntd.0000368
                2631131
                19190771
                Lv et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 8
                Categories
                Research Article
                Ecology
                Infectious Diseases/Infectious Diseases of the Nervous System
                Public Health and Epidemiology/Infectious Diseases

                Infectious disease & Microbiology

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